Secular changes in eruption of primary teeth in Chinese infants and young children from three national cross-sectional surveys

The eruption of primary teeth is a basic event during physical development of children, which is affected by heredity and environment. This study aimed to analyze the changes in primary teeth eruption among Chinese children with social development. A total of 249,264 healthy children under 2 years were extracted from the 1995, 2005, and 2015 National Survey on the Physical Growth and Development of Children in Nine Cities of China. Their primary teeth were examined and percentiles of primary teeth eruption age were calculated by probit analysis. The median primary teeth eruption age were 6.8 months, 6.7 months, 6.6 months in 1995, 2005 and 2015. Primary teeth eruption age of boys was 0.2 months, 0.3 months, 0.3 months earlier than that of girls in 1995, 2005 and 2015. Primary teeth eruption age was the earliest in children from northern region and was the latest in children from southern region, and this regional difference did not change over time. These findings suggest that primary teeth eruption age slightly advanced with social development, and their gender difference and regional difference have always existed, which supplied some data for understanding the secular trend of primary teeth development in stomatology, pediatrics, anthropology, and other related fields.


Participants and sample size
Healthy children under 2 years old who are local residences in the selected region or those who lived in the region for longer than 2/3 of their lifetimes were evaluated for the status of their primary teeth development in the three surveys.The inclusion and exclusion criteria of participants in the three surveys were the same, as reported previously 17 .All children were divided into 12

Ethics approval and consent to participate
The study had been approved by the Ethics Committee of the Capital Institute of Pediatrics (SHERLL2015009).All participations were voluntary and the inform consents were obtained from the parents of all participants after members of the surveys' staff explained to the parents of children the purpose of the survey.Additionally, all methods were performed in accordance with the Declaration of Helsinki.

Data collection and quality control
Primary teeth development was examined in the field by trained investigators using the same method in the three surveys.Primary teeth eruption was defined as having occurred if any part of the primary teeth had, on direct inspection of the mouth, pierced the gum line (clinical emergence).The status of primary teeth eruption was recorded as yes or no in the customized questionnaire and the total number of erupted primary teeth was also recorded.Furthermore, weight, length and head circumference were measured by investigators using the standardized method, and other related information (paternal demographic data, breastfeeding, complementary feeding) was obtained by interview in person.All investigators participated in rigorous specialized training prior to collection of data and passed an examination before the survey.5% of total subjects in each site were measured repeatedly at random each day, and the proportion of subjects beyond allowable errors was less than 10%.

Statistical analysis
Data analysis was done using the Statistical Package for the Social Sciences (SPSS) software, version 22 (developed by SPSS Inc. in Chicago, IL, USA).Z scores of weight, length, head circumference and BMI were calculated by LMS method using the WHO standards (2006).All the basic characteristics were expressed as frequencies for categorical data and‾x ± SD for quantitative data, and their corresponding comparison among the three NSPGDC (III-V) were analyzed by χ 2 or Analysis of Variance (ANOVA) method.Comparison of the primary teeth eruption prevalence in each age group among the NSPGDC III-V was carried out by linear-by-linear association χ 2 method.The probit regression analysis, the conventional way to determine the age of transition into any developmental stage which was used to determine the cumulative percentage of subjects by month or year of age entering into the developmental stage as has been previously described 18 , was performed to calculate the percentiles (the 3rd, 10th, 25th, 50th, 75th, 90th and 97th) of eruption age of primary teeth.The median and the quartiles values (Q1,Q3) of the number of erupted primary teeth were calculated and their comparison among the three surveys was analyzed by the independent sample Kruskal-Wallis Test.The eruption age of the primary teeth and the number of erupted primary teeth were compared with descriptive methods in 1995, 2005 and 2015, which detailed the secular changes of primary teeth development for Chinese infant and young children.A value of P < 0.05 was considered statistically significant.

Basic characteristics of participants in the NSPGDC III-V, 1995-2015
The basic characteristics of participants in 1995, 2005 and 2015 is shown in Table 2.We found there was no statistical difference in the proportions of gender or regions in the three surveys.The level of parental education significantly improved during the two decades and the family income also increased during the lasted decade.Birth weight of participants slightly increased from 1995 to 2015.In addition, the length and weight of children significantly increased during the two decades.The BMI and head circumference increased significantly in the first decade and their changes were not obvious in the second decade.

Changes in eruption age of primary teeth
Table 4 shows the median age of primary teeth eruption was 6.8 months in 1995, 6.7 months in 2005, and 6.6 months in 2015, which declined 0.2 months during the two decades.The relative change of the median age of primary teeth eruption was 2.9% (calculated by "the changes during 1995-2015 divided by the value in 1995, 0.2 months/6.8months * 100").Furthermore, the decrement of the 3rd and 97th percentile age of primary teeth eruption was respectively 0.1 months and 0.3 months during the two decades.
Figure 1 shows that the median age of primary teeth eruption of boys were 6.7 months in 1995, 6.6 months in 2005 and 6.4 months in 2015, and those of girls were 6.9 months in 1995, 6.9 months in 2005 and 6.7 months in 2015.Throughout the three surveys, the primary teeth eruption age of boys were earlier than that of girls, and the gender difference was always remain, such as 0.2 months in 1995 and 0.3 months in 2015.
Figure 2 shows that the eruption age of primary teeth was the earliest in children from the northern region and the latest in the southern region in the three surveys, and the difference between the northern and southern region was 0.5-0.6 months from 1995 to 2015.

Changes in number of erupted primary teeth in the same age group from 1995 to 2015
Table 5 shows the number of erupted primary teeth in each age group in 1995, 2005 and 2015, whose difference were statistical significance at 7 m ~ group to 15 m ~ group during 1995-2015.For example, the median of the number of erupted primary teeth at 10 m ~ group was 4 in 1995, 5 in 2005 and 5 in 2015.Figure 3 shows the proportion of the number of erupted primary teeth in each age group in the three surveys, which illustrated that the proportion of infants with more number of erupted primary teeth in the same group was higher in 2015 than that in 1995, for example, the proportion of 0 erupted teeth, 1-2 erupted teeth, 3-6 erupted teeth and ≥ 6 erupted teeth was respectively 20.0%, 40.9%, 33.1% and 6.0% in 1995, and 18.1%, 39.1%, 35.6% and 7.1% in 2015 (P = 0.000).

Discussions
Under the background of the secular trend of physical growth in children, it is also critical to understand whether there is a short-term or long-term change in the primary teeth eruption for the evaluation of tooth development, the formulation of early prevention policies for dental caries and other anthropological studies.In the present study, we observed a change in primary teeth eruption from 1995 to 2015 in Chinese infants and young children.
The prevalence of primary teeth eruption from 1995 to 2015 increased slightly in infants aged 5 ~ 10 months, but it did not significantly change in infants under 5 months and older than 12 months.These results suggested that early or delayed eruption of primary teeth was not common in infants in the two decades, but more infants aged 5 ~ 10 months have erupted primary tooth today than those of 20 years ago.Furthermore, we found that the median eruption age of primary teeth has declined from 1995 to 2015.A similar secular trend was observed in Polish children 14 and in Caucasian infants from Arizona 11 .However, other reports showed a delayed trend in Indian 15 and Egyptian infants 13 .Whether the differences in the secular trends of primary teeth development  to the advance of the age of late primary teeth eruption and the narrowing of the range of eruption age.It is suggested that the primary teeth eruption will advance with social development, economic improvement and nutritional improvement during pregnancy and infancy, especially the situation of delayed teeth eruption will be significantly improved.Furthermore, we found that the relative changes of the median age of primary teeth eruption were 2.9%.However, a systematic review showed that the age of breast development in Chinese girls advanced with a relative change of 6.1% (0.6 years/9.8 years * 100) over 17 years 5 , and the age of menarche in Chinese girls advanced with a relative change of 7.0% (0.94 years old/13.41years old * 100) over 25 years 22 .It can thus be seen that the relative change of eruption age of primary teeth was lesser than other physical development indicators, which suggest that the effect of social environment on primary teeth development may be weaker and then its secular changes showed a smaller trend.
Surveys in Canada 23 , the United States 11 , Spain 24 and Poland 14 have shown that the eruption age of primary teeth in boys is slightly earlier than that in girls, and this gender difference is related to the different hormone levels between genders during fetal dentition development 25 .Similar results were also found in our study, and the changes in gender difference of primary teeth eruption age were not obvious.The results suggested that the gender difference of primary teeth development may be mainly related to physiological differences between genders and may not change significantly with environment.
There are obvious regional differences in physical growth of Chinese children 17 .In the present study, we also found that the regional difference in the primary teeth eruption age, which illustrated that the primary teeth eruption age in the northern region is earlier than that in the southern region, and this regional difference does not narrow with time.Other data from China also indicated the similar regional difference, for example, the eruption age of primary teeth in Gansu province (7 months) in northern China 26 was earlier than that in Hong Kong (8.2 months) 27 and Chongqing (8 months) in the south 28 .The regional differences in primary teeth development may be related to the great differences in climate, living environments, cultural customs, eating habits, parental somatotypes in different regions.
In addition to the eruption age, the number of erupted primary teeth are also important.We found that the proportion of infants with more number of erupted primary teeth in the same group became higher over the two decades, which suggested that the number of erupted primary teeth in the same age group increased.A recent report in Japan shows that the mean number of emerged primary teeth decreased between 1980 and 2012, and believed that this trend associated to the decrease of birth weight and weight and height at 18 months old 16 .The difference in changes of the number of emerged primary teeth may relate to the increment of birth weight, length and weight of infants in our study.It was indicated that the number of erupted primary teeth will increase with nutritional improvement during pregnancy and infancy, which suggested that oral health care should be paid attention to as early as possible in infants with good nutritional status to prevent the occurrence of dental caries.
There remain some limitations in this study.First, the cross-sectional survey method was used to calculate the eruption age of primary teeth, which may be bias compared with the data obtained from longitudinal studies, as well as the sequence and duration of primary teeth eruption were not considered.Long-term longitudinal studies are difficult to implement, so we only discussed the changes of the eruption age of the primary teeth in different time using the cross-sectional surveys like most population studies.Second, considering the feasibility and the accuracy of information collection in large-scale population surveys, we only investigated the number of erupted primary teeth of infants and young children, but did not record the position of the primary teeth.Third, we only analyzed the trends of primary teeth eruption among infants and young children under 24 months because the primary teeth erupted data was not collected among young children above 24 months in 1995, which may not cover all trends of primary teeth eruption because of around 28-32 months for all the primary teeth erupted.
In conclusion, the primary teeth eruption slightly advanced with social development, and their gender difference and regional difference have always existed, which supplied some data for understanding the secular trend of primary teeth development in anthropology and other related fields, and supplied some evidence for evaluating primary teeth eruption and formulating policies in the oral health care and the early prevention of dental caries in stomatology and pediatrics.In the future, more primary teeth development data from various populations based on the same research methods is necessary to clarify whether there is an advanced trend and their related factors.

Figure 1 .
Figure 1.The median eruption age of primary teeth in boys and girls from 1995 to 2015.The error bar was the 95%CI of the median eruption age of primary teeth.

Figure 2 .
Figure 2. The median eruption age of primary teeth in northern, central and southern regions from 1995 to 2015.The error bar was the 95%CI of the median eruption age of primary teeth.
Table 1 shows sex-age subgroup sample sizes.

Table 3
shows that the prevalence of primary teeth eruption in the age group of 5 ~ 10 months groups increased from 1995 to 2015 (P = 0.000 ~ 0.036), while its changes in other age groups from 1995 to 2015 were no statistical significance.

Table 3 .
Changes of prevalence of primary teeth eruption in different age groups.n refer to the number of children whose primary teeth had erupted, % refer to the prevalence of primary teeth eruption in the age group.

Table 4 .
Changes of the percentiles of primary teeth eruption age.